A non-avian dinosaur with a streamlined body exhibits potential adaptations for swimming

Streamlining a body is a major adaptation for aquatic animals to move efficiently in the water. Whereas diving birds are well known to have streamlined bodies, such body shapes have not been documented in non-avian dinosaurs. It is primarily because most known non-avian theropods are terrestrial, barring a few exceptions. However, clear evidence of streamlined bodies is absent even in the purported semiaquatic groups. Here we report a new theropod, Natovenator polydontus gen. et sp. nov., from the Upper Cretaceous of Mongolia. The new specimen includes a well-preserved skeleton with several articulated dorsal ribs that are posterolaterally oriented to streamline the body as in diving birds. Additionally, the widely arched proximal rib shafts reflect a dorsoventrally compressed ribcage like aquatic reptiles. Its body shape suggests that Natovenator was a potentially capable swimming predator, and the streamlined body evolved independently in separate lineages of theropod dinosaurs.

characters shared with other halszkaraptorines [9,24]. The forelimb elements are partially 158 exposed (Figs. 1a, b, 2a-d, 3e, g). The humerus appears to be short. The shaft of the ulna is 159 mediolaterally compressed to produce a sharp posterior margin as in Halszkaraptor[9] and 160 Mahakala [24]. Metacarpal III is robust and is only slightly longer than metacarpal II. 161 Similarly, metacarpal III is almost as thick and long as other second metacarpals of other 162 halszkaraptorines [9,24]. The femur has a long ridge on its posterior surface, which is another 163 character shared among halszkaraptorines [9]. Typically for a dromaeosaurid, metatarsals II 164 and III have ginglymoid distal articular surfaces (Fig. 3h, Extended Data Fig. 4f, h). The with Halszkaraptor (Fig. 3i), forelimbs probably were the primary source of propulsion when 213 swimming, as has been suggested for the latter [9]. Furthermore, the aquatic adaptations in 214 Natovenator help resolve the debate on the ecology of Halszkaraptor [17,41]. The previous 215 argument that Halszkaraptor represents a transitional taxon rather than a semiaquatic one [41] 216 can be refuted because the streamlined body and other specializations of Natovenator 8 concretely support the semiaquatic ecology of Halszkaraptor. 218 The morphology of Natovenator also provides vital information for understanding 219 the body plan of halszkaraptorines because it has many anatomical characters previously 220 restricted to Halszkaraptor, including the shared ecological indicators described here. Some 221 of these traits, especially those in the proximal caudal vertebrae, are shared with Mahakala 222 [24]. It is also notable that Natovenator is from the Baruungoyot Formation, whereas 223 Halszkaraptor is from the Djadochta beds. The striking similarities between Natovenator and   To investigate the relationships of Natovenator with other theropods, a phylogenetic analysis 249 was conducted using a revised data matrix from Cau[19], which is based on that of Cau et 250 al. [9]. The modifications that were made in the data matrix are the addition of Natovenator, 251 removal of four taxa (Alnashetri, Shanag, Fukuivenator, and Hesperornithoides) to prevent 252 collapses of major clades, two-character scorings of Mahakala regarding parapophyses of 253 dorsal vertebrae (character 238; from 0 to 1) and the existence of a fibular notch on the 254 calcaneum (character 1430; from ? to 1) based on the description of this taxa from Turner et 255 al. [24]. As a result, 182 taxa with 1807 characters (four ordered) were incorporated in our 256 matrix, then analyzed via TNT ver 1.5 [43]. The maximum number of trees was set to 99,999, 257 and Herrerasaurus was used as the outgroup taxon. A "New Technology Search" including 258 "Sect. Search" (with RSS, CSS, and XSS checked), "Ratchet," "Drift," and "Tree fusing" was 259 performed with default parameters, followed by the final round of "Traditional Search," also 260 with default parameters, to further explore the shortest trees. Bremer support values at each 261 node were calculated using the Bremer.run script.                                          To Reviewer #1 1 Referee comment Reply Overall this manuscript is in very good shape and I have only very minor concerns and comments about it (and not too many of them). See attached marked up document for these.
There is however one major and serious issue that needs to be fully addressed. A major part of the argument about this paper is that the laterally directed ribs is linked to a) streamlining and b) specifically based on the form seen in diving birds. However, support for this contention is essentially non-existent.
On line 204-205 you cite 3 papers to support this contention (you 7, 36 & 37). I checked all three of these and found the following -the first of these only cites the other two as a source for this point about rib angles and so really isn't independent. Both the other two only make simple statements 'rib angle is linked to streamlining and diving in birds' without themselves providing any data or evidence for the point at all. They are unsupported statements without even giving the nature of this observation (e.g. 'our examination of numerous diving birds shows that...).
As such, there is no actual evidence for this at all and if you intend to argue that this animal was a diver based on rib angles this needs actual support and these papers do not provide it. You'll need to actually survey and measure diving birds and nondivers and see if the rib angle does correlate with diving. Even then, I'm not sure you can argue that this is specifically about streamlining without any actual We would like to thank Reviewer #1 for his/her critical comments on our manuscript. Reviewer #1 raised an issue on our interpretation of the dorsal rib orientation related to a streamlined body. Our response to this concern is as follows.
First, Reviewer #1 commented "A major part of the argument about this paper is that the laterally directed ribs is linked to a) streamlining and b) specifically based on the form seen in diving birds." While the ribs are (postero)laterally flared out and make the body dorsoventrally compressed, this is not what we argued that streamlines the body. Instead, the streamlined body is formed by the posterior orientation of the ribs as stated in our manuscript (lines 204-212; The dorsal ribs of Natovenator are directed posterolaterally to a significant extent (Figs. 3e, 4a-d). Therefore, the angle between each rib shaft and its associated articulating vertebra is very low, like many diving birds, but in contrast to terrestrial theropods ( Fig. 4e-k, Table 1). A similar condition is known in the semi-or fully aquatic archosauromorph Tanystropheus [32]. Furthermore, certain extant diving birds -such as alcids [33] and phalacrocoracids[34] -also have posteriorly extending ribs. In these animals, backward-oriented ribs aid swimming by making the body more streamlined [35,36]. It is natural because the posterior orientation of the ribs lowers the dorsoventral height of the body, especially posterior to the middle.). The rib angles show degrees of posterior orientation, not lateral orientation. It would not be streamlining if the ribs were only laterally oriented.
Second, Reviewer #1 commented "On line 204-205 you cite 3 papers to support this contention (you 7, 36 & 37). I checked all three of these and found the following -the first of these only cites the other two as a source for this point about rib angles and so really isn't independent. The other two only make simple statements 'rib angle is linked to streamlining and diving in birds' without themselves providing any data or evidence for the point. They are unsupported statements without even giving the nature of this observation (e.g. 'our examination of numerous diving birds shows that...)." We agree that the reference 7 is not independent and removed it. shows the diving bird razorbill (C) with a more streamlined body has lower rib angles. Posterior orientation of ribs streamlines the body because its dorsoventral height is naturally lowered. We added this as the following sentence (lines 211-212; This is natural because the posterior orientation of the ribs lowers the dorsoventral height of the body, especially posterior to the middle.). evidence given then a dorsally compressed body should produce more drag than one with a circular cross-section so that needs to be discussed and explored too.
To be clear, I am not saying this is wrong, but it is unsupported and given how central it is to the arguments here this needs to be addressed properly.
Third, Reviewer #1 commented "You'll need to actually survey and measure diving birds and non-divers and see if the rib angle does correlate with diving." We actually did measure several diving birds, and the rib angles are included in Table 1  (originally Extended Data Table 1). These birds have a streamlined body with posteriorly oriented ribs (lower rib angle). We added rib morphology and angles of some nondivers (Struthio camelus, the common ostrich and Shri devi, a dromaeosaurid from the Baruungoyot Formation) that do not have streamlined bodies to Fig. 4 (j, k) and Table 1, respectively.
Lastly, Reviewer #1 commented "Even then, I'm not sure you can argue that this is specifically about streamlining without any actual evidence given then a dorsally compressed body should produce more drag than one with a circular crosssection, so that needs to be discussed and explored too." Again, we did not state the streamlining results just from a dorsoventral compression. Additionally, Reviewer #1's statement "a dorsally compressed body should produce more drag than one with a circular cross-section" is not true because a circle is always broader than an ellipse given the same circumference, hence less drag on the latter.

Referee comment
Reply The authors describe a new specimen of We thank Reviewer#3 for his/her valuable halzkaraptorine dromaeosaurid, which helps clarify some aspects of the anatomy of this recently discovered and somewhat enigmatic taxon. The new specimen includes skeletal elements not available or not well preserved in previously described individuals.
In particular, the new anatomical features revealed support the earlier hypothesis that halszkaraptorines were adapted to a semi-aquatic mode of life, perhaps more so than other nonavian dinosaurs. Some features of the skull found in Natavenator and in Halskaraptor, for instance, but lacking in typical dromaeosaurids are also found in water-dwelling birds. It is worth noting, however, that retraction of the external naris by itself is not necessarily an aquatic adaptation, or at least not a subaquatic one. As discussed in Hone and Holtz (2021) it is dorsal placement of the naris rather than posterior retraction that is indicative of a subaqueous mode of locomotion.
Hone, D.W.E., and T.R. Holtz, Jr. 2021. Evaluating the ecology of Spinosaurus: shoreline generalist of aquatic pursuit specialist? Palaeontologia Electronica 24(1): a03. doi: 10.26879/1110 comments on our manuscript. Following the Reviewer#3's comment regarding the nares, we added their relative dorsal placement to the description and discussion sections of the main manuscript (lines 58 (dorsolateral placement of retracted external nares), 98 and 99 (It is also dorsally placed compared to those of other nonavian theropods and faces dorsolaterally.), and 191 (retracted and dorsolaterally facing external nares)).
The evidence of the morphology and orientation of the dorsal ribs is particularly interesting, since as the authors note this indicates a streamlined body form as in semiaquatic birds.
The detailed anatomical descriptions provided mostly in the Supplementary data, and the phylogenetic analysis, are sufficient to demonstrate this is a new taxon. The illustrations and data tables are all necessary to support the conclusions of the text. That said, a photograph or drawing of the orientation of the ribs in a nonstreamlined theropod (especially one from the Baruungoyot) might be useful to contrast the position of those compared to Natovenator and the modern aquatic birds.
Following this comment of Reviewer #3, we added a likely terrestrial (not streamlined) dromaeosaurid theropod (Shri devi from the Baruungoyot Formation) to Fig. 4 (Fig. 4k).
It might be worthwhile for the authors to describe the geological/sedimentological setting of the discovery and the support for the subaqueous nature of the deposition at the locality. (Given that this is a morphological/phylogenetic paper it is understandable that these geological issues are not the primary focus. However, perhaps in a future work, that information might be provided to help clarify the environment in which this purported aquatic hunter lived.) We cited Eberth (2018) (reference 13), which gives information on the sedimentology and palaeoenvironment of the Baruungoyot Formation (as well as the Nemegt Fm.). As of now, there is no particularly new sedimentological information we can add to our manuscript. As Reviewer #3 commented, however, it will be worthwhile to examine the site that yielded the new specimen and gather more information on the geological setting.
A non-scientific, but etymological, question: is the name properly formed? Other compound words I can think of derived from "nato" take the form "nata-" (as in "natatorium" for "swimming pool" or "natatorial" for "adapted to swimming). You might want to check with etymology and taxonomy expert Ben Creisler (bcreisler@gmail.com) to check, in case you don't have any Latin experts among the team.
We consulted Ben Creisler as suggested, but he said that Natovenator should be fine. To quote him, he said "The spelling Natovenator to mean "swimming hunter" from the Latin verb nato "swim" should be fine. It is similar to some other generic names formed with a Latin verb. A spelling "natavenator" would not work in this case.". Following his reply, we decided to use the name 'Natovenator' as it is.  Halszkaraptor from the Djadochta Formation of this region revealed its semiaquatic ecology, which is unique among non-avian maniraptorans [9]. Its morphological specializations include 32 a snout with a complex neurovascular network, retracted nares, a dental arrangement for 33 capturing evasive prey, an unusually long neck similar to that of known aquatic reptiles, and      fenestra. The pterygoid is missing its anterior portion (Fig. 2g, Extended Data Fig. 2a-e). A 120 deep fossa on the medial surface of the thin quadrate ramus is not seen in any other 121 dromaeosaurids. The mandibles of Natovenator preserve most of the elements, especially 122 those on the left side (Fig. 1a, b, d, Extended Data Figs. 1a, 2). Each jaw is characterized by a 123 slender dentary with nearly parallel dorsal and ventral margins, a surangular that is partially 124 5 fused with the articular, a distinctive surangular shelf, and a fan-shaped retroarticular process 125 that protrudes dorsomedially. The upper dentition of Natovenator is heterodont as the 126 premaxillary teeth are morphologically distinct from the maxillary teeth (Fig. 2a, b, e, 127 Extended Data Fig. 1a, c). There are unusually numerous premaxillary teeth that are tightly  The neck of Natovenator as preserved is twisted and includes ten elongate cervical 139 vertebrae, although most of the 5th cervical is missing (Figs. 1, 3a-d). This elongation of the 140 cervicals results in a noticeably longer neck than those of most dromaeosaurids and is 141 estimated to be longer than the dorsal series. It is, however, relatively shorter than that of 142 Halszkaraptor, which has a neck that is half of its precaudal length [9]. Another peculiarity in 3e, 4a-d). They are also nearly horizontal, which is indicative of a dorsoventrally compressed 6 ribcage. Each of the proximal caudal vertebrae has a long centrum and horizontal 156 zygapophyses with expanded laminae (Fig. 3f, Extended Data Fig. 3e-i), all of which are 157 characters shared with other halszkaraptorines[9, 24]. The forelimb elements are partially 158 exposed (Figs. 1a, b, 2a-d, 3e, g). The humerus appears to be short. The shaft of the ulna is and III have ginglymoid distal articular surfaces (Fig. 3h, Extended Data Fig. 4f, h). The   There is also a trend among modern birds that aquatic taxa possess long necks, presumably 196 related to feeding habits and bracing impacts during dives [33]. Additionally, Natovenator 197 provides additional insight into its semiaquatic ecology with its dorsal rib morphology. The                                        Halszkaraptor from the Djadochta Formation of this region revealed its semiaquatic ecology, 2 which is unique among non-avian maniraptorans[9]. Its morphological specializations include 32 a snout with a complex neurovascular network, retracted nares, a dental arrangement for 33 capturing evasive prey, an unusually long neck similar to that of known aquatic reptiles, and  The skull of Natovenator is nearly complete, although the preorbital region has been 98 affected by compression and is slightly offset from the rest of the skull (Figs. 1c, d, 2a-d,   99 Extended Data Figs. 1, 2). Near the tip of the snout, the premaxilla is marked by a broad 100 groove. The body of the premaxilla is also dorsoventrally low and is perforated by numerous 101 foramina that lead into a complex network of neurovascular chambers (Extended Data Fig. 1b) 102 as in Halszkaraptor[9]. Similarly, the external naris is positioned posteriorly and is level with 103 the premaxilla-maxilla contact (Fig. 2a, b), although it is marginally behind this position in  Fig. 2a-e). The latter also produces a shelf that extends over fenestra. The pterygoid is missing its anterior portion (Fig. 2g, Extended Data Fig. 2a-e). A 120 deep fossa on the medial surface of the thin quadrate ramus is not seen in any other 121 dromaeosaurids. The mandibles of Natovenator preserve most of the elements, especially 122 those on the left side (Fig. 1a, b, d, Extended Data Figs. 1a, 2). Each jaw is characterized by a 123 slender dentary with nearly parallel dorsal and ventral margins, a surangular that is partially 124 5 fused with the articular, a distinctive surangular shelf, and a fan-shaped retroarticular process 125 that protrudes dorsomedially. The upper dentition of Natovenator is heterodont as the 126 premaxillary teeth are morphologically distinct from the maxillary teeth (Fig. 2a, b, e, 127 Extended Data Fig. 1a, c). There are unusually numerous premaxillary teeth that are tightly  The neck of Natovenator as preserved is twisted and includes ten elongate cervical 139 vertebrae, although most of the 5th cervical is missing (Figs. 1, 3a-d). This elongation of the 140 cervicals results in a noticeably longer neck than those of most dromaeosaurids and is 141 estimated to be longer than the dorsal series. It is, however, relatively shorter than that of 142 Halszkaraptor, which has a neck that is half of its precaudal length [9]. Another peculiarity in 3e, 4a-d). They are also nearly horizontal, which is indicative of a dorsoventrally compressed 6 ribcage. Each of the proximal caudal vertebrae has a long centrum and horizontal 156 zygapophyses with expanded laminae (Fig. 3f, Extended Data Fig. 3e-i), all of which are 157 characters shared with other halszkaraptorines [9,24]. The forelimb elements are partially 158 exposed (Figs. 1a, b, 2a-d, 3e, g). The humerus appears to be short. The shaft of the ulna is and III have ginglymoid distal articular surfaces (Fig. 3h, Extended Data Fig. 4f, h). The  There is also a trend among modern birds that aquatic taxa possess long necks, presumably 196 related to feeding habits and bracing impacts during dives [33]. Additionally, Natovenator 197 provides additional insight into its semiaquatic ecology with its dorsal rib morphology. The           angular; at, atlas; ax, axis; dr, dorsal rib; dtr, dorsal tympanic recess; p, parietal; pop, 437 paroccipital process; pt, pterygoid; q, quadrate; qj, quadratojugal; oc, occipital condyle; 438 rp, retroarticular process; sa, surangular; sc, scapula; sq, squamosal; so, supraoccipital.      I have only one major issue still and that is the idea of rib angle being linked to diving. I am happy with the idea that the ribs you have here are orientated like those of diving ducks and auks. What you did not demonstrate before, and still have not demonstrated, is that the angle of these ribs directly contributes to streamlining. The only evidence you were able to provide was the three references all of which essentially stated that this was true but themselves without evidence. There is no actual direct evidence in the literature (e.g. a formal study of the distribution of rib shape and behavior, or that compressed ribs increases streamlining) and therefore this remains an unsupported assertion, not anything with actual evidence. You say for example that the razorbill has the more streamlined body in Fig 1 of Tickle et al. but how is this demonstrated? Again there is no actual evidence, you can't look at a skeleton and declare it more streamlined. Even the correlation here hasn't been reasonably demonstrated. Pointing out that an ostrich and dromaeosaur have different ribs really doesn't add to this argument. To be clear, I strongly suspect you are correct. But the interpretation of halszkaraptorines as being semi-aquatic has been contentious and this is a major argument being put forwards for this behavior and the evidence you have for this is, to my mind, extraordinarily weak. It's pointing to a handful of very grossly similar animals that have some putative behaviours in common and stating that X directly leads to Y and you simply don't have the evidence to support that. You need a much stronger case and I don't think it's unreasonable to ask you do a serious survey of the literature and / or some actual specimens and demonstrate this association rather than infer it from a couple of papers that themselves state it without support.

This needs fixing.
To Reviewer #1 1

Referee comments
Reply I have only one major issue still and that is the idea of rib angle being linked to diving. I am happy with the idea that the ribs you have here are orientated like those of diving ducks and auks. What you did not demonstrate before, and still have not demonstrated, is that the angle of these ribs directly contributes to streamlining. The only evidence you were able to provide was the three references all of which essentially stated that this was true but themselves without evidence. There is no actual direct evidence in the literature (e.g. a formal study of the distribution of rib shape and behavior, or that compressed ribs increases streamlining) and therefore this remains an unsupported assertion, not anything with actual evidence. You say for example that the razorbill has the more streamlined body in Fig 1 of Tickle et al. but how is this demonstrated? Again there is no actual evidence, you can't look at a skeleton and declare it more streamlined. Even the correlation here hasn't been reasonably demonstrated. Pointing out that an ostrich and dromaeosaur have different ribs really doesn't add to this argument.
To be clear, I strongly suspect you are correct. But the interpretation of halszkaraptorines as being semi-aquatic has been contentious and this is a major argument being put forwards for this behavior and the evidence you have for this is, to my mind, extraordinarily weak. It's pointing to a handful of very grossly similar animals that have some putative behaviours in common and stating that X directly leads to Y and you simply don't have the evidence to support that. You need a much stronger case and I don't think it's unreasonable to ask you do a serious survey of the literature and / or some actual specimens and demonstrate this association rather than infer it from a couple of papers that themselves state it without support. This needs fixing.
Our response to the comments from Reviewer #1 is as follows.
In our previous response and revised manuscript, we stated how posteriorly oriented ribs contribute to streamlining the body (by lowering the dorsoventral height). A streamlined body is a posteriorly tapering body, and the posterior orientation of ribs, in contrast to the vertical orientation, naturally helps make this shape. Of course, not all aquatic animals have ribs with strong posterior orientations, but as far as we know, all animals with posteriorly oriented ribs have hydrodynamic body profiles.
Reviewer #1 commented, "You say, for example, that the razorbill has the more streamlined body in Fig 1 of Tickle et al., but how is this demonstrated?". Because the bird is extant, and it is known that it has a streamlined body, the skeleton helps us understand how they have such a body shape.
We previously provided several clades of diving birds as examples for comparison. Although we believe what we presented was good enough, we added more examples and elaboration (lines 208-217: This is natural because the posterior orientation of the ribs lowers the dorsoventral height of the body and lengthens the rib cage. The resulted long rib cage then contributes to streamlining the body in diving birds [34]. In addition to diving birds, the semiaquatic modern platypus[35] and possible semiaquatic archosauromorph Tanystropheus[36] also possess ribs that extend posteriorly. On the other hand, the ribs in fully aquatic tetrapods such as mosasaurs and extant cetaceans are posteriorly oriented relative to the long axis of the body partly because of inclined thoracic vertebrae, and the anterior migration of the rib cage and abdominal organs is also instrumental in streamlining their bodies[37-41]. Consequently, Natovenator acquired a similar rib profile to that of semiaquatic amniotes (Table 2).).